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1 Fine-Scale Adaptations to Environmental Variation and Growth 1 Strategies Drive Phyllosphere Methylobacterium Diversity. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.04.447128; this version posted July 7, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 FINE-SCALE ADAPTATIONS TO ENVIRONMENTAL VARIATION AND GROWTH 2 STRATEGIES DRIVE PHYLLOSPHERE METHYLOBACTERIUM DIVERSITY. 3 4 Jean-Baptiste Leducq1,2,3, Émilie Seyer-Lamontagne1, Domitille Condrain-Morel2, Geneviève 5 Bourret2, David Sneddon3, James A. Foster3, Christopher J. Marx3, Jack M. Sullivan3, B. Jesse 6 Shapiro1,4 & Steven W. Kembel2 7 8 1 - Université de Montréal 9 2 - Université du Québec à Montréal 10 3 – University of Idaho 11 4 – McGill University 12 13 Key words: Methylobacterium diversity, Phyllosphere community dynamics, rpoB barcoding, 14 temperature adaptation, growth strategies in Bacteria 15 16 Abstract 17 Methylobacterium is a prevalent bacterial genus of the phyllosphere. Despite its ubiquity, little is 18 known about the extent to which its diversity reflects neutral processes like migration and drift, 19 or environmental filtering of life history strategies and adaptations. In two temperate forests, we 20 investigated how phylogenetic diversity within Methylobacterium was structured by 21 biogeography, seasonality, and growth strategies. Using deep, culture-independent barcoded 22 marker gene sequencing coupled with culture-based approaches, we uncovered a previously 23 underestimated diversity of Methylobacterium in the phyllosphere. We cultured very different 24 subsets of Methylobacterium lineages depending upon the temperature of isolation and growth 25 (20 °C or 30 °C), suggesting long-term adaptation to temperature. To a lesser extent than 26 temperature adaptation, Methylobacterium diversity was also structured across large (>100km; 27 between forests) and small geographical scales (<1.2km within forests), among host tree species, 28 and was dynamic over seasons. By measuring growth of 79 isolates at different temperature 29 treatments, we observed contrasting growth performances, with strong lineage- and season- 30 dependent variations in growth strategies. Finally, we documented a progressive replacement of 31 lineages with a high-yield growth strategy typical of cooperative, structured communities, in 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.04.447128; this version posted July 7, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 32 favor of those characterized by rapid growth, resulting in convergence and homogenization of 33 community structure at the end of the growing season. Together our results show how 34 Methylobacterium is phylogenetically structured into lineages with distinct growth strategies, 35 which helps explain their differential abundance across regions, host tree species, and time. This 36 works paves the way for further investigation of adaptive strategies and traits within a ubiquitous 37 phyllosphere genus. 38 39 Abstract importance 40 Methylobacterium is a bacterial group tied to plants. Despite its ubiquity and importance to their 41 hosts, little is known about the processes driving Methylobacterium community dynamics. By 42 combining traditional culture-dependent and –independent (metagenomics) approaches, we 43 monitored Methylobacterium diversity in two temperate forests over a growing season. On the 44 surface of tree leaves, we discovered remarkably diverse and dynamic Methylobacterium 45 communities over short temporal (from June to October) and spatial scales (within 1.2 km). 46 Because we cultured very different subsets of Methylobacterium diversity depending on the 47 temperature of incubation, we suspected that these dynamics partly reflected climatic adaptation. 48 By culturing strains in lab conditions mimicking seasonal variations, we found that diversity and 49 environmental variations were indeed good predictors of Methylobacterium growth 50 performances. Our findings suggest that Methylobacterium community dynamics at the surface of 51 tree leaves results from the succession of strains with contrasted growth strategies in response to 52 environmental variations. 53 54 Acknowledgments: FRQNT (funding), NSERC (funding), Canada Research Chairs (funding), 55 NSF (DEB-1831838), Geneviève Lajoie, Dominique Tardif, Ariane Lafrenière, Hélène Dion- 56 Phénix, Yves Terrat, Kenta Araya (help for sampling), Sylvain Dallaire (help for phenotyping 57 screen), Sergey Stolyar (discussions), Gault Natural Reserve (McGill University), Station 58 Biologique des Laurentides (UdeM), Centre d’Étude de la Forêt (CEF), QCBS. 59 60 Author contributions : J.B.L., E.S.L., D.C.M., G.B., B.J.S. and S.W.K. planned fieldwork and 61 the experiments. J.B.L. E.S.L., D.C.M. and G.B. performed experiments. J.B.L., E.S.L., D.S. and 62 J.M.S performed bioinformatic analyses. J.A.F., C.J.M. and J.M.S. provided discussion in the 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.04.447128; this version posted July 7, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 63 early stages of this study. J.B.L. B.J.S. and S.W.K. drafted the manuscript with contributions 64 from C.J.M. 65 66 Data accessibility: raw reads for 16s and rpoB barcoding on phyllosphere communities 67 (BioProject PRJNA729807; BioSamples SAMN19164946-SAMN19165146) were deposited in 68 NCBI under SRA Accession Numbers SRR14532212-SRR14532451. Partial nucleotide 69 sequences from marker genes obtained by SANGER sequencing on Methylobacterium isolates 70 (BioProject PRJNA730554 ; Biosamples SAMN19190155-SAMN19190401) were deposited in 71 NCBI under GenBank Accession Numbers MZ268514-MZ268593 (16s), MZ330152-MZ330358 72 (rpoB) and MZ330130-MZ330151 (sucA). R codes and related data were deposited on Github 73 (https://github.com/JBLED/methylo-phyllo-diversity). 74 75 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.04.447128; this version posted July 7, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 Introduction 77 78 Phyllosphere, the aerial parts of plants including leaves, is a microbial habitat estimated as vaste 79 as twice the surface of the earth (1). Although exposed to harsh conditions, like UVs, temperature 80 variations and poor nutrient availability, the phyllosphere arbors a diverse community of 81 microorganisms, of which bacteria are the most abundant (1). A key challenge in microbial 82 ecology and evolution is understanding the evolutionary and ecological processes that maintain 83 diversity in habitats such as the phyllosphere. Bacteria living in the phyllosphere carry out key 84 functions including nitrogen fixation, growth stimulation and protection against pathogens (1–3). 85 At broad spatial and temporal scales, bacterial diversity in the phyllosphere varies as a function 86 of biogeography and host plant species, potentially due to restricted migration and local 87 adaptation to the biotic and abiotic environment (4–6), leading to patterns of cophylogenetic 88 evolutionary association between phyllosphere bacteria and their host plants (7). Whether those 89 eco-evolutionary processes are important at short time scales, as microbes and their host plants 90 migrate and adapt to changing climates, is still an open question (8). Another challenge is to link 91 seasonal variation with plant-associated microbial community dynamics, as shifts in microbial 92 community composition are tighly linked with host plant carbon cycling (9) and ecosystem 93 functions including nitrogen fixation (10). More generally, we understand very little about how 94 the ecological strategies of phyllosphere bacteria vary among lineages and in response to 95 variation in environmental conditions throughout the growing season (9, 11). 96 97 Phylogenetic signal in traits or suites of correlated traits that are used as indicators of the 98 ecological life history strategy of microbes suggest niche adaptation (12), and these phenotypic 99 traits influence the assembly of ecological communities through their mediation of organismal 100 interactions with the abiotic and biotic environment (13). Recent work evaluating the 101 phylogenetic depth of microbial trait evolution has shown that many microbial phenotype traits 102 exhibit phylogenetic signal, with closely related lineages possessing similar phenotypic traits, 103 although the phylogenetic depth at which this signal is evident differs among traits (14). Most 104 comparative studies of microbial trait evolution have focused on broad scale patterns across 105 major phyla and classes (14), although some studies have found evidence for complex patterns of 106 phenotypic and genomic evolution within microbial genera interacting to determine patterns of 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.04.447128; this version posted July 7, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 107 community assembly and niche evolution (15, 16). Furthermore, to date the majority of studies of 108 the diversity of plant-associated microbes have been based on the use of universal marker genes 109 such as the bacterial 16S rRNA gene, providing
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